Báo cáo lâm nghiệp: "Interactions between root symbionts, root pathogens and actinorhizal plants"

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Interactions between root symbionts, root pathogens and actinorhizal plants Akkermans, D. Hahn ; F. Zoon A. Department of Microbiology, Wageningen Agricutural University, Wageningen, The Netherlands tion of plants with Frankia is dependent Introduction upon the environmental conditions, in- cluding the interaction with other soil microorganisms (van Dijk, 1984; Houwers and Akkermans, 1981; Maas et al., 1983; Actinorhizal trees with acti- nitrogen-fixing Oremus, 1980, Oremus and Otten, 1981 ). nomycetes (Frankia sp.) microsym- as These results indicate that plant growth is bionts in root nodules play an important often limited by factors other than N fixa- 2 ecological role as pioneer plants on nitro- tion. gen-poor soils. Up to 200 perennial spe- cies, alltrees and shrubs, distributed over Each soil ecosystem comprises a large about 20 genera, have been found to be number of different types of organisms nodulated with Frankia as the nodule sym- with a complex network of interactions. biont. Some of those, e.g., Alnus spp. in Tree growth is therefore affected by inter- temperate regions and Casuarina spp. in action with many different types of organ- subtropical and tropical regions, have isms. In soil, the roots are in close contact great potentials for biomass production with pathogenic fungi, nematodes and and erosion control (Silvester, 1977). The insects, but also with symbiotic organ- growth of such plants is largely dependent isms, such as mycorrhizal fungi, rhizo- upon the presence of proper Frankia bacteria and nodule-forming Frankia. strains in the soil. Although Frankia has Although the importance of such interac- been found in many types of soil, particu- tions is generally recognized in forestry, larly in soils where its host plants have little attention has been paid to their effect been grown previously (Fraga-Beddiar, on nitrogen-fixing actinorhizal plants. In 1987; Houwers and Akkermans, 1981; the present paper, we will give an over- Rodriguez-Barrueco, 1968), inoculation of view of the interactions between root sym- the plants with selected Frankia strains bionts, pathogens and actinorhizal plants, can give a positive response with respect with special attention to Alnus and Hippo- to plant yield. Pot and field experiments have indicated that the effect of inocula- phae spp.
tion to this host-induced ineffectivity, Fran- Root symbionts kia strains which lack nitrogenase have been found in soil (van Dijk and Sluimer- Frankia Stolk, 1984) and pure cultures of these ineffective strains have been described (Hahn et aL, 1988; Hahn et aL, 1989). plants bear several types of Actinorhizal their roots. So far, most symbionts on After initial invasion of the cortical cells, attention has been paid to microorganisms Frankia readily develops into an endosym- nitrogen-fixing root nodules which induce biont with vesicles at the hyphal tips. The (i.e., actinorhizas). Although it has been form of these vesicles is largely deter- known for about a century that the micro- mined by the host plant, and varies from in nodules of, e.g., Elaeagnus, symbionts spherical (e.g., in root nodules of Alnus Alnus and Casuarina are different from and Hippophae, spp.) to club- or pear- Rhizobium in leguminous nodules, pure shaped (e.g., Myrica and Comptonia spp.). cultures of the microsymbionts have only So far, Frankia strains usually form spheri- been available since 1978 (Callaham et cal vesicles in pure culture and no alterna- al., 1978). These microbes are classified tive forms have been observed in vitro. within the genus Frankia. Frankia is char- Host-controlled morphogenesis has also acterized by its hyphal growth type, anal- been observed in the spore-formation of ogous to many other actinomycetes. It Frankia. So far, isolated Frankia strains forms typical intercalar and terminal spo- are usually able to produce sporangia, rangia and vesicles at the tips of short side depending upon the medium. In the branches. These 2 structures are unique nodules, however, strains fail to form spo- to the genus Frankia and can be used as rangia. Field studies by van Dijk have indi- morphological markers in the identification cated the presence of 3 types of nodules of the microbes, excluding, however, inef- in Alnus glutinosa, viz. spore-positive fective and non-infective strains. (i.e., spore-forming) types, spore-negative After local colonization of the roots of types, in which ino spores are visible, and actinorhizal plants, Frankia strains invade ineffective nodules, which contain non- the plants either through deformed root nitrogen-fixing endophytes which are only hairs, e.g., in Alnus spp. or through inter- present in the hyphal form (van Dijk, 1984; cellular spaces, as has been demon- van Dijk and Sluimer-Stolk, 1984). Cross- strated in Elaeagnus sp. (Miller and Baker, inoculation experiments by van Dijk have 1986). These observations indicate that at clearly demonstrated that this feature is least 2 types of invasions exist in actino- dependent upon the type of strain and not rhizal plants. on the plant. The occurrence of spore- positive nodule:;, has also been discov- Pure cultured Frankia strains can be ered recently in A. incana, A. rugosa and classified into 3 groups, based on host- Myrica gale and the ecology of the strains specificity, viz. Alnus- compatible, Elae- has been investigated. Spatially distinct agnus!compatible and Casuarina!ompat- distribution patterns of the spore (+) and ible strains (Baker, 1987). The degree of spore (-) types of nodules indicate that nitrogen-fixing activity in the nodules both strains have distinct ecological pre- varies with the host plant and the Frankia ferences. Chemical analysis of isolates of strain. Strains which are effective (i.e., N - 2 types of Frankia strains indicates both fixing) on its original host, may be ineffec- tive (non-N on other hosts within differences which permit taxo- significant -fixing) 2 nomic distinction between Frankia alni the same cross-inoculation group. In addi-
subspecies Pommeri (spore-negative) and ly stimulated the N activity by ing X -f’ 2 Frankia on Hippophae (Gardner et al., subspecies Vandijkii (spore-positive) (Lalonde, 1988). Unfortunately, only very 1984). Although most VA-endomycorrhi- few spore-positive Frankia strains, if any, zas are generally non-specific, recent have been obtained in pure culture and observations by Fraga-Beddiar (1987) indicate the existence of host-specific the ability to sporulate within the nodules types on A. glutinosa in acid soil. has not always been well documented. Over the last decennium, several thou- Ectomycorrhizas have been found in sand Frankia strains have been isolated. nature and the associations have been The results have been reported or sum- synthesized in vitro (reviewed by Gardner, marized at the various conferences and 1986). Fraga-Beddiar (1987) observed workshops on Frankia and actinorhizal that ecomycorrhizal fungi invade the roots of alder at a late stage, i.e., after initial al., 1984; Huss- plants (Akkermans et Danell and Wheeler, 1987; Lalonde et al., infections by endomycorrhizal fungi and Frankia. Field and laboratory observations 1985; Torrey and Tjepkema, 1983). Identi- fication and characterization of these indicate that the genus Alnus may express strains have been made on the basis of strong specialization regarding its ectomy- corrhizal fungal partners (Matsui, 1926, morphological features, host-specificity, Neal et al., 1968; Mejstrik and Benecke, nitrogen-fixing ability, protein pattern, lipid composition or DNA characteristics 1969; Molina, 1979). Since Alnus rubra intermixed with Douglas fir results in a (Normand et al., 1988; Simonet et al., 1988; 1989). Promising techniques for reduction of the population of the root identification have also been found in the pathogen fungus Poria weirri, it has been analysis of unique sequences in the 16S suggested that this is due to the presence rRNA (Hahn et al., 1989). of obligate mycorrhizal symbionts that antagonize the pathogen (Trappe, 1972). As will be shown later, various other expla- Endo- and ectomycorrhizal fungi nations have been given to explain this phenomenon. Both endo- and ectomycorrhizal fungi are known to occur in actinorhizal plants and Rhizobacteria have a direct effect on the growth of the plants. In some soils, mycorrhizal fungi are highly abundant and may compete with In addition to Frankia and mycorrhizas, Frankia for sites on the roots. The occur- several other microorganisms have been rence and role of actinorhizal-mycorrhizal suggested to influence the growth of the associations have recently been summa- plants positively producing plant-stimu- rized by Daft et aL (1985) and Gardner lating growth hormones and anti-microbial (1986). Some actinorhizal plants, such as compounds. So far, specific root associa- Hippophae, predominantly contain VA tions with rhizobacteria and actinorhizal (endo)mycorrhizal fungi, while others, plants have been described only occasion- e.g., Alnus spp., contain both endo- and ally. Recently, Dobritsa and Sharaya ectomycorrhizal fungi. Various findings (1986) isolated H Nocardia -consuming 2 indicate their role in the uptake of phos- autotrophica from the roots and nodules of phate and their antagonistic effect on root Alnus glutinosa and proposed an interest- pathogens. In soil low in both N and P, ing new type of tripartite interaction in Glomus fasciculatus VA-mycorrhiza great- which the H formed by the nodules is 2
recycled by Nocardia. It is likely that this available the of this physiology on asso- kind of symbiosis is most effective with ciation. uptake hydrogenase-negative Frankia Red alder (Alnus rubra) is resistant to strains which are unable to recycle the H2 infection by Poria weirii, one of the major produced by nitrogenase. root pathogens of conifers in western North America (Wallis and Reynolds, 1962; 1965). In addition to the involvement of specific ectomycorrhizas, as described Root pathogens above, this phenomenon has also been explained by competition for available have a significant Although pathogens nitrogen. Soils under red alder trees effect on tree growth in managed forests, contain high levels of nitrate, which cannot little attention has been given to their be utilized by I’oria as a nitrogen source effect on actinorhizal plants. Our basic (Li et al., 1968). Moreover, the presence of knowledge of the plant-parasite relation- polyphenoloxidases in alder tissue which ship in natural ecosystems is therefore oxidizes adihydric phenol into fungitoxic extremely limited. Several actinorhizal compounds may explain the resistance to plants, e.g., Alnus, Hippophae and Casu- Poria (Li et al., 1968). It has been sug- arina form monocultures as pioneer gested that either Alnus or its root nodule vegetation, which degenerate after a pe- symbiont, Frankia, exudes anti-fungal riod of time. Our observations indicate that compounds which suppress Poria sp. pathogens may be involved in this pro- Alder plants may contain various toxic cess, as will be described below. Reduc- compounds, including polyphenols and tion of pathogens can often yield greater antibiotics. The exudation of bactericides economic profit than inoculation with by Alnus glutinosa has been reported (Sei- Frankia alone, particularly when native del, 1972) and ii: has been applied in purifi- Frankia populations are already present. cation plants with polluted waste water from hospitals. The anti-microbial effects of plant polyphenols have been reported Fungi and it is likely that this will largely explain these phenomena. In addition, it has been shown that some Frankia strains exude Several fungi have been described to be anti-fungal and anti-bacterial compounds pathogenic to the roots of actinorhizal under axenic conditions (Akkermans, plants. Pythium spp. (oomycetes) which unpublished). Their ecological role, how- form zoospores are potent root killers that ever, is unknown. often occur in moist soils. Several Penicillium strains have been The influence of pathogenic fungi on the found to form myconodules on the roots of growth of Hippophae has been demon- Alnus glutinosa (Capellano et aL, 1987; strated by treatment of the soils with beno- van Dijk, 1984; van Dijk and Sluimer-Stolk, myl (against hyphomycetes) and propa- 1984). This interesting new type of asso- mocarb (against oomycetes) (Zoon, in ciation occurs in certain soils and may preparation). The effect of these com- affect plant growth, either by competition pounds on pathogenic fungi is dependent for nutrients or by competition with Fran- upon the soil type. In young sandy dune kia for infection sites on the roots (van soils with Hippaphae vegetation, addition Dijk, 1984; van Dijk and Sluimer-Stolk, of benomyl resulted in a 2-fold increase 1984). Nevertheless, little information is of nodule number/plant. In older soils
plant parasite Tylenchorynchus micro- (60-100 yr old dune area) with degener- phasmis Loof, which occurs in much ating Hippophae vegetations, addition of higher densities. Pot experiments in which benomyl resulted in a 10-fold increase in Tylenchorynchus is added to the soil show nodule number/plant. These soils often contain Cylindrocarpon spp. and Fusa- damaging effects on the plants (Zoon, rium oxysporum as the major rhizosphere manuscript in preparation) similar to those and root fungi. Similar treatments of old seen in field studies. With increasing num- soils (ca 200 yr) with degenerated Hippo- bers of nematodes added per pot, the phae vegetations, had less effect, proba- number of nodules per unit of root length decreases. In addition, the total root bly because other organisms had more effect on plant growth as will be shown length decreases. Chemical analysis of below. The impact of Pythium (oomycetes) the plants shows a decreased P content in some of the soils has been demon- and a slightly increased N content of the shoots. Since P uptake, in contrast to N strated by the addition of propamocarb (20 mg/kg dry soil). Other studies on the effect uptake, is highly determined by the size of benomyl application to soils had and activity of the root system, the effect demonstrated that a reduction of the fun- of nematodes on the size of the root gal population in the rhizosphere resulted system mainly results in reduced P uptake in an increase in the population of actino- by the plant. mycetes in the rhizosphere. The positive The effect of nematodes on plant growth effect of benomyl on nodulation might and nodulation of Hippophae has also therefore be explained either by a direct been demonstrated by the addition of oxa- stimulation of Frankia in the rhizosphere myl, a nematostatic compound, to soil or indirectly by changing the microbial samples. Addition of oxamyl to soil interactions in the rhizosphere (van Faa- samples from both vigorous and degen- ssen, 1974). This needs further studies. erating Hippophae vegetations, generally containing T. microphasmis, significantly improves the number of nodules formed Nematodes per seedling, indicating that nematode effects occur on most field sites. Field stu- dies demonstrate that plant parasites Field studies on nodulation of Hippophae increase in numbers in older Hippophae in England (Stewart and Pearson, 1967) vegetations, while available soil phospho- and The Netherlands (Akkermans, 1971; rus and total plant production decrease. It Oremus, 1980) indicated that shrubs in old is tempting to suggest that nematodes dune areas were often badly nodulated play a significant role in the degeneration and degenerated rapidly. Subsequent pot of the shrubs (Zoon, 1986). experiments have shown that soils under degenerated Hippophae shrubs contain plant parasitic nematodes which seriously affect the growth of Hippophae seedlings, Concluding remarks in spite of the presence of Frankia (Ore- 1980; Oremus and Otten, 1981; mus, Maas et al., 1983; Zoon, in preparation). the last decennia, foresters have During Special attention in these studies was paid much information on the growth of gained to the large plant parasitic nematode Lon- natural stands of economically important gidorus dunensis (Brinkman et al.) which actinorhizal plants, e.g., Alnus spp. Phy- occurs in low numbers and the smaller siologists have gained information on the
Baker D.D. (1987) Relationships among pure effect of abiotic factors on plant growth cultured strains of Frankia based on host speci- and soil microbiologists have recognized ficity. Physiol. Plant. 70, 245-248 the role of root symbionts and pathogens Callaham D., dell Tredici P. & Torrey J.R. (1978) in the growth of the plants. Combination of Isolation and cultivation in vitro of the actinomy- the knowledge obtained in different disci- cete causing root nodulation in Comptonia. plines is needed in order to understand Science 199, 899-902 the complexity of the interactions between Capellano A., Dequatre B., Valla G. & Moiroud plants, microbes, small animals and A. (1987) Root-nodule formation by Penicillium sp. on Alnus glutinosa and Alnus incana. Plant their environment. This multidisciplinary Soil 104, 45-51 approach will help us to improve wood Daft, M.J., Clelland D.M. & Gardner I.C. (1985) production and will give new ways for Symbiosis with endomycorrhizas and nitrogen- controlling tree growth. fixing organisms. Proc. R. Soc. Edinburgh 85B, 283-298 in this paper The overview presented Dobritsa S.V. & Sharaya L.S. (1985) Genome indicates that our information about root identity of different Nocardia autotrophica iso- interactions is fragmentary and has to be lates from Alnus spp. root nodules and rhizo- improved in the near future. The examples In: Proceedings of the Sixth Int. Symp. sphere. demonstrate that several root symbionts on Actinomycetes Biology (Szabo G., Biro S. & are host-specific, which opens up the Goodfellow M., eds.), Acad. Kiado, Budapest, pp. 735-737 opportunity to manipulate the system. Fraga-Beddiar A,. (1987) Interactions entre les Introduction of selected or even genetical- symbiotes mycorhiziens et les symbiotes fixa- ly engineered mycorrhizal fungi or Fran- teurs d’azote chez I’aulne glutineux (Alnus glu- kia can be used for biological control of tinosa (L.) Gaertn. Ph.D. Thesis, Université de root pathogens and for improvement of Nancy, France symbiotic nitrogen fixation in forestry. Gardner I.C. (1986) Mycorrhizae of actinorhizal plants. MIRCEN J. Appl. MicrobioL Biotechnol. 2, 147-160 Gardner I.C., Cl!elland D.M. & Scott A. (1984) Mycorrhizal improvement in non-leguminous Acknowledgments nitrogen-fixing associations with particular refer- ence to Hippophae rhamnoides L. Plant Soil 78, 189-199 The investigators were supported by the Foun- Hahn D., Dorsch M., Stackebrandt E. & Akker- dation for Fundamental Biological Research (BION), which is subsidized by the Netherlands mans A.D.L. (1989) Synthetic oligonucleotide probes for identification of Frankia strains. Organization for Scientific Research (NWO) Plant Soil, 118, 211-219 and the Commission of the European Commu- 9 nities (EEC) (no. EN3B-0043-NL (GDF)). Hahn D., Starrenburg M.J.C. & Akkermans A.D.L. (1988) Variable compatibility of cloned Alnus glutinosa ecotypes against ineffective Frankia strains. Plant Soil 107, 233-243 Houwers A. & Akkermans A.D.L. (1981 ) Influ- References ence of inoculation on yield of Alnus glutinosa in The Netherlands. Plant Soil 61 , 189-202 Akkermans A.D.L. (1971) Nitrogen fixation and Huss-Danell K. & Wheeler C.T (1987) Frankia nodulation of Alnus glutinosa and Hippophae and actinorhizal plants. Physiol. Plant. 70, 235- rhamnoides under natural conditions. Thesis, 377 University of Leiden, The Netherlands Lalonde M. (1988) Advances in the taxonomy of Frankia: recognition of species Alni and Elae- Akkermans A.D.L., Baker D., Huss-Danell K. & agni and novel subspecies pommerii and van- In: Tjepkema J.D. (1984) Frankia Symbioses. dijkii. In: Nitrogen Fixation: A Hundred Years Developments in Plant and Soil Sciences 12 After, Proc. 7th Int. Congress on Nitrogen Fixa- (Plant Soil, 78, nos. 1-2)
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